Physiological response to membrane protein overexpression in E. coli

Molecular and Cellular Proteomics

Volumn 10, Issue 10, 2011, Pages

  Gubellini, Francesca ^a,c   Verdon, Grégory ^a,d   Karpowich, Nathan K ^a,e   Luff, Jon D ^a   Boël, Grégory ^a   Gauthier, Nils ^a,f   Handelman, Samuel K ^a,g   Ades, Sarah E ^b   Hunt, John F ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c INSTITUT PASTEUR   (France)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^g OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; TRANSCRIPTOME; ESCHERICHIA COLI PROTEIN; MESSENGER RNA; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL CELL; BIOGENESIS; CELL GROWTH; CRYSTALLIZATION; ESCHERICHIA COLI; GENE INACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; BIOSYNTHESIS; CHEMISTRY; GENE EXPRESSION REGULATION; GENE VECTOR; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METHODOLOGY; PROTEIN MICROARRAY;

ESCHERICHIA COLI;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC VECTORS; MEMBRANE PROTEINS; PROTEIN ARRAY ANALYSIS; PROTEIN FOLDING; RNA, MESSENGER; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 80054016202     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M111.007930     Document Type: Article

References (50)

1. Gordon, E., Horsefield, R., Swarts, H. G., de Pont, J. J., Neutze, R., and Snijder, A. (2008) Effective high-throughput overproduction of membrane proteins in Escherichia coli. Protein Expr. Purif. 62, 1-8
2. Wagner, S., Baars, L., Ytterberg, A. J., Klussmeier, A., Wagner, C. S., Nord, O., Nygren, P. A., van Wijk, K. J., and de Gier, J. W. (2007) Consequences of membrane protein overexpression in Escherichia coli. Mol. Cell Proteomics 6, 1527-1550 (Pubitemid 47506165)
3. Wagner, S., Klepsch, M. M., Schlegel, S., Appel, A., Draheim, R., Tarry, M., Högbom, M., van Wijk, K. J., Slotboom, D. J., Persson, J. O., and de Gier, J. W. (2008) Tuning Escherichia coli for membrane protein overexpression. Proc. Natl. Acad. Sci. U.S.A. 105, 14371-14376
4. Wang, D. N., Safferling, M., Lemieux, M. J., Griffith, H., Chen, Y., and Li, X. D. (2003) Practical aspects of overexpressing bacterial secondary membrane transporters for structural studies. Biochim. Biophys. Acta 1610, 23-36 (Pubitemid 36173993)
5. White, S. H. (2009) Biophysical dissection of membrane proteins. Nature 459, 344-346
6. White, S. H., and von Heijne, G. (2008) How translocons select transmembrane helices. Annu. Rev. Biophys. 37, 23-42
7. von Heijne, G. (2011) Introduction to theme "membrane protein folding and insertion". Annu. Rev. Biochem. 80, 157-160
8. Dalbey, R. E., Wang, P., and Kuhn, A. (2011) Assembly of bacterial inner membrane proteins. Annu. Rev. Biochem. 80, 161-187
9. Junge, F., Schneider, B., Reckel, S., Schwarz, D., Dötsch, V., and Bernhard, F. (2008) Large-scale production of functional membrane proteins. Cell Mol. Life Sci. 65, 1729-1755
10. Schlegel, S., Klepsch, M., Gialama, D., Wickström, D., Slotboom, D. J., and de Gier, J. W. (2010) Revolutionizing membrane protein overexpression in bacteria. Microb. Biotechnol. 3, 403-411
11. Yosef, I., Bochkareva, E. S., Adler, J., and Bibi, E. (2010) Membrane protein biogenesis in Ffh- or FtsY-depleted Escherichia coli. PLoS One 5, e9130
12. Yosef, I., Bochkareva, E. S., and Bibi, E. (2010) Escherichia coli SRP, Its Protein Subunit Ffh, and the Ffh M Domain Are Able To Selectively Limit Membrane Protein Expression When Overexpressed. MBio 1
13. Katzen, F., Peterson, T. C., and Kudlicki, W. (2009) Membrane protein expression: no cells required. Trends Biotechnol. 27, 455-460
14. Drew, D., Fröderberg, L., Baars, L., and de Gier, J. W. (2003) Assembly and overexpression of membrane proteins in Escherichia coli. Biochim. Biophys. Acta 1610, 3-10 (Pubitemid 36173991)
15. Geertsma, E. R., and Poolman, B. (2010) Production of membrane proteins in Escherichia coli and Lactococcus lactis. Methods Mol. Biol. 601, 17-38
16. Laage, R., and Langosch, D. (2001) Strategies for prokaryotic expression of eukaryotic membrane proteins. Traffic 2, 99-104 (Pubitemid 32219862)
17. Miroux, B., and Walker, J. E. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298 (Pubitemid 26254109)
18. Arechaga, I., Miroux, B., Karrasch, S., Huijbregts, R., de Kruijff, B., Runswick, M. J., and Walker, J. E. (2000) Characterisation of new intracellular membranes in Escherichia coli accompanying large scale over-production of the b subunit of F(1)F(o) ATP synthase. FEBS Lett. 482, 215-219
19. Weiner, J. H., Lemire, B. D., Elmes, M. L., Bradley, R. D., and Scraba, D. G. (1984) Overproduction of fumarate reductase in Escherichia coli induces a novel intracellular lipid-protein organelle. J. Bacteriol. 158, 590-596 (Pubitemid 14147629)
20. Wilkison, W. O., Bell, R. M., Taylor, K. A., and Costello, M. J. (1992) Structural characterization of ordered arrays of sn-glycerol-3-phosphate acyltransferase from Escherichia coli. J. Bacteriol. 174, 6608-6616
21. Chen, Y., Song, J., Sui, S. F., and Wang, D. N. (2003) DnaK and DnaJ facilitated the folding process and reduced inclusion body formation of magnesium transporter CorA overexpressed in Escherichia coli. Protein Expr. Purif. 32, 221-231 (Pubitemid 38039013)
22. Link, A. J., Skretas, G., Strauch, E. M., Chari, N. S., and Georgiou, G. (2008) Efficient production of membrane-integrated and detergent-soluble G protein-coupled receptors in Escherichia coli. Protein Sci. 17, 1857-1863
23. Massey-Gendel, E., Zhao, A., Boulting, G., Kim, H. Y., Balamotis, M. A., Seligman, L. M., Nakamoto, R. K., and Bowie, J. U. (2009) Genetic selection system for improving recombinant membrane protein expression in E. coli. Protein Sci. 18, 372-383
24. Zweers, J. C., Wiegert, T., and van Dijl, J. M. (2009) Stress-responsive systems set specific limits to the overproduction of membrane proteins in Bacillus subtilis. Appl. Environ. Microbiol. 75, 7356-7364
25. Ulbrandt, N. D., Newitt, J. A., and Bernstein, H. D. (1997) The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88, 187-196 (Pubitemid 28015867)
26. Gill, R. T., Valdes, J. J., and Bentley, W. E. (2000) A comparative study of global stress gene regulation in response to overexpression of recombinant proteins in Escherichia coli. Metab. Eng. 2, 178-189
27. Smith, H. E. (2007) The transcriptional response of Escherichia coli to recombinant protein insolubility. J. Struct. Funct. Genomics 8, 27-35
28. Boël, G., Pichereau, V., Mijakovic, I., Mazé, A., Poncet, S., Gillet, S., Giard, J. C., Hartke, A., Auffray, Y., and Deutscher, J. (2004) Is 2-phosphoglycerate-dependent automodification of bacterial enolases implicated in their export? J. Mol. Biol. 337, 485-496
29. Costanzo, A., and Ades, S. E. (2006) Growth phase-dependent regulation of the extracytoplasmic stress factor, sigmaE, by guanosine 3′,5′- bispyrophosphate (ppGpp). J. Bacteriol. 188, 4627-4634 (Pubitemid 43956060)
30. Doerrler, W. T., Reedy, M. C., and Raetz, C. R. (2001) An Escherichia coli mutant defective in lipid export. J. Biol. Chem. 276, 11461-11464
31. Miller, J. (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory, NY
32. Huang, Y., Lemieux, M. J., Song, J., Auer, M., and Wang, D. N. (2003) Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301, 616-620 (Pubitemid 36927940)
33. Ward, A., Reyes, C. L., Yu, J., Roth, C. B., and Chang, G. (2007) Flexibility in the ABC transporter MsbA: Alternating access with a twist. Proc. Natl. Acad. Sci. U.S.A. 104, 19005-19010
34. Sharp, M. D., and Pogliano, K. (1999) An in vivo membrane fusion assay implicates SpoIIIE in the final stages of engulfment during Bacillus subtilis sporulation. Proc. Natl. Acad. Sci. U.S.A. 96, 14553-14558 (Pubitemid 30000688)
35. Aung, S., Shum, J., Abanes-De Mello, A., Broder, D. H., Fredlund-Gutierrez, J., Chiba, S., and Pogliano, K. (2007) Dual localization pathways for the engulfment proteins during Bacillus subtilis sporulation. Mol. Microbiol. 65, 1534-1546 (Pubitemid 47347834)
36. Ades, S. E. (2008) Regulation by destruction: design of the sigmaE envelope stress response. Curr. Opin. Microbiol. 11, 535-540
37. Mecsas, J., Rouviere, P. E., Erickson, J. W., Donohue, T. J., and Gross, C. A. (1993) The activity of sigma E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins. Genes Dev. 7, 2618-2628
38. Hayden, J. D., and Ades, S. E. (2008) The extracytoplasmic stress factor, sigmaE, is required to maintain cell envelope integrity in Escherichia coli. PLoS One 3, e1573
39. Raivio, T. L. (2005) Envelope stress responses and Gram-negative bacterial pathogenesis. Mol. Microbiol. 56, 1119-1128
40. Parsell, D. A., and Sauer, R. T. (1989) Induction of a heat shock-like response by unfolded protein in Escherichia coli: dependence on protein level not protein degradation. Genes Dev. 3, 1226-1232
41. De Wulf, P., Kwon, O., and Lin, E. C. (1999) The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of unanticipated target operons. J. Bacteriol. 181, 6772-6778 (Pubitemid 29517993)
42. Anderson, J. K., Smith, T. G., and Hoover, T. R. (2010) Sense and sensibility: flagellum-mediated gene regulation. Trends Microbiol. 18, 30-37
43. Sharma, U. K., and Chatterji, D. (2010) Transcriptional switching in Escherichia coli during stress and starvation by modulation of sigma activity. FEMS Microbiol. Rev. 34, 646-657
44. Srivatsan, A., and Wang, J. D. (2008) Control of bacterial transcription, translation and replication by (p)ppGpp. Curr. Opin. Microbiol. 11, 100-105
45. Baev, M. V., Baev, D., Radek, A. J., and Campbell, J. W. (2006) Growth of Escherichia coli MG1655 on LB medium: monitoring utilization of sugars, alcohols, and organic acids with transcriptional microarrays. Appl. Microbiol. Biotechnol. 71, 310-316 (Pubitemid 43962135)
46. Baev, M. V., Baev, D., Radek, A. J., and Campbell, J. W. (2006) Growth of Escherichia coli MG1655 on LB medium: determining metabolic strategy with transcriptional microarrays. Appl. Microbiol. Biotechnol. 71, 323-328 (Pubitemid 43962137)
47. Baev, M. V., Baev, D., Radek, A. J., and Campbell, J. W. (2006) Growth of Escherichia coli MG1655 on LB medium: monitoring utilization of amino acids, peptides, and nucleotides with transcriptional microarrays. Appl-.Microbiol. Biotechnol. 71, 317-322 (Pubitemid 43962136)
48. Vanderpool, C. K. (2007) Physiological consequences of small RNA-mediated regulation of glucose-phosphate stress. Curr. Opin. Microbiol. 10, 146-151
49. Kaberdin, V. R., and Lin-Chao, S. (2009) Unraveling new roles for minor components of the E. coli RNA degradosome. RNA Biol. 6, 402-405
50. Nonaka, G., Blankschien, M., Herman, C., Gross, C. A., and Rhodius, V. A. (2006) Regulon and promoter analysis of the E. coli heat-shock factor, sigma32, reveals a multifaceted cellular response to heat stress. Genes Dev. 20, 1776-1789 (Pubitemid 43992886)